Genetic and functional diversity help explain pathogenic, weakly pathogenic, and commensal lifestyles in the genusXanthomonas

Abstract

The genusXanthomonashas been primarily studied for pathogenic interactions with plants. However, besides host and tissue specific pathogenic strains, this genus also comprises nonpathogenic strains isolated from a broad range of hosts, sometimes in association with pathogenic strains, and other environments, including rainwater. Based on their incapacity or limited capacity to cause symptoms on the host of isolation, nonpathogenic xanthomonads can be further characterized as commensal and weakly pathogenic. This study aimed to understand the diversity and evolution of nonpathogenic xanthomonads compared to their pathogenic counterparts based on their co-occurrence and phylogenetic relationship and to identify genomic traits that form the basis of a life-history framework that groups xanthomonads by ecological strategies. We sequenced genomes of 83 strains spanning the genus phylogeny and identified eight novel species, indicating unexplored diversity. While some nonpathogenic species have experienced a recent loss of a type III secretion system, specifically, thehrp2cluster, we observed an apparent lack of association of thehrp2cluster with lifestyles of diverse species. We gathered evidence for gene flow among co-occurring pathogenic and nonpathogenic strains, suggesting the potential of nonpathogenic strains to act as a reservoir of adaptive traits for pathogenic strains and vice versa. We further identified traits enriched in nonpathogens that suggest a strategy of stress tolerance, rather than avoidance, during their association with a broad range of host plants.

Characterization of Xanthomonas hortorum isolates causing leaf spot on Primula vulgaris

“…These possibilities have been proposed in the course of the evolution of epiphytes and pathogens. The community formed by bacteria with different lifestyles could serve as a gene pool with the potential to contribute to gene exchange, evolution and emergence of new pathogens (Bansal et al, 2020;Cesbron et al, 2015;Lee et al, 2020;Pena et al, 2023;te Molder et al, 2021). The diminished occurrence may not be considered as unexpected as is concomitant with reductions in the habitat diversity and coverage of the native Primula spp.…”

Xanthomonas rydalmerensis sp. nov., a non-pathogenic member of Group 1 Xanthomonas

“…These three NCBI isolates have not previously been classified as representing a species of the genus Xanthomonas and do not share an ANI exceeding 95 % with any isolates of known species of the genus Xanthomonas. Isolates 3307 and 3498 were collected from rainwater in the USA and LMG9002 was collected in 1989 from an orange tree in the USA and has been confirmed to be non-pathogenic [40,41].…”

Xanthomonas sontii, and notXanthomonas sacchari, is the dominant, vertically transmitted core rice seed endophyte

“…The genus Xanthomonas is primarily known as a pathogen of a wide range of plants infecting in the host and the tissue-specific manner [16]. However, in recent decades, there have been increasing reports of NPX strains from different plants [17]. For example, in rice, only one pathogenic species, X. oryzae , has been known for last 100 years [18].…”